Advertisement

Evolutionary Ecology

, Volume 33, Issue 1, pp 21–36 | Cite as

Nesting on high: reproductive and physiological consequences of breeding across an intertidal gradient

  • Aneesh P. H. BoseEmail author
  • Brittney G. Borowiec
  • Graham R. Scott
  • Sigal Balshine
Original Paper

Abstract

Nest site selection is a critical parental decision with profound fitness consequences, yet the physiological consequences of these decisions are rarely examined. Certain fishes and other aquatic organisms construct nests and provide parental care in the intertidal zone—an environment characterized by fluctuating water levels, which can exert intermittent and sometimes extreme abiotic stress on the animals that live there including dramatic changes in temperature and dissolved oxygen level. In this study, we used the plainfin midshipman fish, Porichthys notatus, to test whether (1) nest site preferences and reproductive success vary across an intertidal elevation gradient, and (2) fish that nest at higher elevations pay greater physiological costs due to prolonged exposure to more extreme abiotic conditions. We found that fish preferred nests lower in the intertidal zone, with larger males outcompeting smaller males for these sites. Broods at high elevations suffered greater offspring mortality than broods at lower elevations. The average microhabitat temperature of nests was also warmer and more variable at higher elevations compared to lower elevations. While isolated from the ocean during low tides, care-giving parents increased their use of anaerobic metabolism, and potentially draw upon oxygen reserves in the swim bladder. Our results suggest that the choice of nesting location can have profound effects on a parent’s physiology and may generate significant variation in reproductive success among individuals.

Keywords

Abiotic stress Parental care Beach spawning Nest site selection Male competition Toadfish 

Notes

Acknowledgements

We are indebted to Chuck and Sally Flader as well as Eileen Carr and family for providing lodging and access to the field sites. We also thank J. Miller, N. Houpt, E. Sadler, N. Brown, M. Lapstra, K. Cogliati, and C. Hiltz for assistance with field work. This work was funded by Natural Sciences and Engineering Research Council of Canada grants to SB and GRS (Grant Nos. 222854-2011 and 418202-2012). Additional funding was provided to AB by the Department of Psychology, Neuroscience and Behaviour at McMaster University. Analyses reported in this article can be reproduced using the data provided in the Supplementary Materials.

Author contributions

AB, SB, BB, and GRS conceived and designed the study. AB and SB conducted the field work. BB conducted the laboratory assays. AB analyzed the data. AB and BB wrote the paper with input from all co-authors.

Compliance with ethical standards

Conflict of interest

No competing interests declared.

Supplementary material

10682_2019_9970_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 16 kb)
10682_2019_9970_MOESM2_ESM.csv (3 kb)
Supplementary material 2 (CSV 4 kb)
10682_2019_9970_MOESM3_ESM.csv (535 kb)
Supplementary material 3 (CSV 535 kb)
10682_2019_9970_MOESM4_ESM.csv (9 kb)
Supplementary material 4 (CSV 10 kb)

References

  1. Arora HL (1948) Observations on the habits and early life history of the batrachoid fish, Porichthys notatus Girard. Copeia 1948(2):89–93.  https://doi.org/10.2307/1438409 CrossRefGoogle Scholar
  2. Bass AH, Marchaterre MA (1989) Sound-generating (sonic) motor system in a teleost fish (Porichthys notatus): sexual polymorphism in the ultrastructure of myofibrils. J Comp Neurol 286(2):141–153.  https://doi.org/10.1002/cne.902860202 CrossRefPubMedGoogle Scholar
  3. Berg T, Steen JB (1965) Physiological mechanisms for aerial respiration in the eel. Comp Biochem Physiol 15(4):469–484.  https://doi.org/10.1016/0010-406X(65)90147-7 CrossRefPubMedGoogle Scholar
  4. Bergmeyer HU (1983) Methods of enzymatic analysis, 3rd edn. Academic Press, New YorkGoogle Scholar
  5. Bermudes M, Ritar AJ (1999) Effects of temperature on the embryonic development of the striped trumpeter (Latris lineata Bloch and Schneider, 1801). Aquaculture 176(3–4):245–255.  https://doi.org/10.1016/S0044-8486(99)00117-9 CrossRefGoogle Scholar
  6. Bose AP, Cogliati KM, Howe HS, Balshine S (2014) Factors influencing cannibalism in the plainfin midshipman fish. Anim Behav 96:159–166.  https://doi.org/10.1016/j.anbehav.2014.08.008 CrossRefGoogle Scholar
  7. Bose AP, McClelland GB, Balshine S (2015) Cannibalism, competition, and costly care in the plainfin midshipman fish, Porichthys notatus. Behav Ecol 27(2):628–636.  https://doi.org/10.1093/beheco/arv203 CrossRefGoogle Scholar
  8. Bose AP, Kou HH, Balshine S (2016) Impacts of direct and indirect paternity cues on paternal care in a singing toadfish. Behav Ecol 27(5):1507–1514.  https://doi.org/10.1093/beheco/arw075 CrossRefGoogle Scholar
  9. Bose AP, Cogliati KM, Luymes N, Bass AH, Marchaterre MA, Sisneros JA, Bolker BM, Balshine S (2018) Phenotypic traits and resource quality as factors affecting male reproductive success in a toadfish. Behav Ecol 29(2):496–507.  https://doi.org/10.1093/beheco/ary002 CrossRefGoogle Scholar
  10. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254.  https://doi.org/10.1016/0003-2697(76)90527-3 CrossRefGoogle Scholar
  11. Brantley RK, Bass AH (1994) Alternative male spawning tactics and acoustic signals in the plainfin midshipman fish Porichthys notatus Girard (Teleostei, Batrachoididae). Ethology 96(3):213–232.  https://doi.org/10.1111/j.1439-0310.1994.tb01011.x CrossRefGoogle Scholar
  12. Cogliati KM, Neff BD, Balshine S (2013) High degree of paternity loss in a species with alternative reproductive tactics. Behav Ecol Sociobiol 67(3):399–408.  https://doi.org/10.1007/s00265-012-1460-y CrossRefGoogle Scholar
  13. Cogliati KM, Danukarjanto C, Pereira AC, Lau MJ, Hassan A, Mistakidis AF, Bolker BM, Neff BD, Balshine S (2015) Diet and cannibalism in plainfin midshipman Porichthys notatus. J Fish Biol 86(4):1396–1415CrossRefPubMedGoogle Scholar
  14. Collette B, Acero A, Betancur R, Cotto A, Rojas P (2010) Porichthys notatus. The IUCN red list of threatened species. Version 2014.3. www.iucnredlist.org. Accessed 21 Nov 2018
  15. Craig PM, Fitzpatrick JL, Walsh PJ, Wood CM, McClelland GB (2014) Coping with aquatic hypoxia: how the plainfin midshipman (Porichthys notatus) tolerates the intertidal zone. Environ Biol Fish 97(2):163–172.  https://doi.org/10.1007/s10641-013-0137-3 CrossRefGoogle Scholar
  16. Crane JM Jr (1981) Feeding and growth by the sessile larvae of the teleost Porichthys notatus. Copeia 1981:895–897.  https://doi.org/10.2307/1444196 CrossRefGoogle Scholar
  17. Davies R, Moyes CD (2007) Allometric scaling in centrarchid fish: origins of intra- and inter-specific variation in oxidative and glycolytic enzyme levels in muscle. J Exp Biol 210:3798–3804.  https://doi.org/10.1242/jeb.003897 CrossRefPubMedGoogle Scholar
  18. DeMartini EE (1988) Spawning success of the male plainfin midshipman. I. Influences of male body size and area of spawning site. J Exp Mar Biol Ecol 121(2):177–192.  https://doi.org/10.1016/0022-0981(88)90254-7 CrossRefGoogle Scholar
  19. DeMartini EE (1991) Spawning success of the male plainfin midshipman. II. Substratum as a limiting spatial resource. J Exp Mar Biol Ecol 146(2):235–251.  https://doi.org/10.1016/0022-0981(91)90028-u CrossRefGoogle Scholar
  20. Dunn JF, Hochachka PW (1986) Metabolic responses of trout (Salmo gairdneri) to acute environmental hypoxia. J Exp Biol 123:229–242Google Scholar
  21. Forstmeier W, Weiss I (2004) Adaptive plasticity in nest-site selection in response to changing predation risk. Oikos 104(3):487–499.  https://doi.org/10.1111/j.0030-1299.1999.12698.x CrossRefGoogle Scholar
  22. Fretwell SD (1972) Populations in a seasonal environment (no. 5). Princeton University Press, PrincetonGoogle Scholar
  23. Kabacoff R (2011) R in action: data analysis and graphics with R. Manning Publications Co., GreenwichGoogle Scholar
  24. LeMoine CM, Bucking C, Craig PM, Walsh PJ (2014) Divergent hypoxia tolerance in adult males and females of the plainfin midshipman (Porichthys notatus). Physiol Biochem Zool 87(2):325–333.  https://doi.org/10.1086/674565 CrossRefPubMedGoogle Scholar
  25. Lisser DF, Lister ZM, Pham-Ho PQ, Scott GR, Wilkie MP (2016) Relationship between oxidative stress and brain swelling in goldfish (Carassius auratus) exposed to high environmental ammonia. Am J Physiol Regul Integr Comp Physiol 312(1):R114–R124.  https://doi.org/10.1152/ajpregu.00208.2016 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Madsen T, Shine R (1999) Life history consequences of nest-site variation in tropical pythons (Liasis fuscus). Ecology 80(3):989–997.  https://doi.org/10.1890/0012-9658(1999)080%5b0989:LHCONS%5d2.0.CO;2 CrossRefGoogle Scholar
  27. Martin KL (1993) Aerial release of CO2 and respiratory exchange ratio in intertidal fishes out of water. Environ Biol Fish 37(2):189–196.  https://doi.org/10.1007/BF00000594 CrossRefGoogle Scholar
  28. Martin KL (2014) Theme and variations: amphibious air-breathing intertidal fishes. J Fish Biol 84:577–602.  https://doi.org/10.1111/jfb.12270 CrossRefPubMedGoogle Scholar
  29. Martin KL, Strathmann R (1999) Aquatic organisms, terrestrial eggs: early development at the water’s edge. Introduction to the symposium. Am Zool 39:215–217CrossRefGoogle Scholar
  30. Martin KL, Swiderski DL (2001) Beach spawning in fishes: phylogenetic tests of hypotheses. Am Zool 41(3):526–537.  https://doi.org/10.1668/0003-1569(2001)041%5b0526:BSIFPT%5d2.0.CO;2 CrossRefGoogle Scholar
  31. Martin KLM, Van Winkle RC, Drais J, Lakisic H (2004) Beach-spawning fishes, terrestrial eggs, and air breathing. Physiol Biochem Zool 77(5):750–759.  https://doi.org/10.1086/421755 CrossRefPubMedGoogle Scholar
  32. Mayer PM, Smith LM, Ford RG, Watterson DC, McCutchen MD, Ryan MR (2009) Nest construction by a ground-nesting bird represents a potential trade-off between egg crypticity and thermoregulation. Oecologia 159(4):893–901.  https://doi.org/10.1007/s00442-008-1266-9 CrossRefGoogle Scholar
  33. Nilsson GE, Östlund-Nilsson S (2008) Does size matter for hypoxia tolerance in fish? Biol Rev 83:173–189.  https://doi.org/10.1111/j.1469-185X.2008.00038.x CrossRefPubMedGoogle Scholar
  34. Perry SF, Braun MH, Genz J, Vulesevic B, Taylor J, Grosell M, Gilmour KM (2010) Acid–base regulation in the plainfin midshipman (Porichthys notatus): an aglomerular marine teleost. J Comp Physiol B 180(8):1213–1225.  https://doi.org/10.1007/s00360-010-0492-8 CrossRefPubMedGoogle Scholar
  35. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2016) _nlme: Linear and nonlinear mixed effects models_. R package version, pp 3.1–128, http://CRAN.R-project.org/package=nlme
  36. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
  37. Raffaelli D, Hawkins S (eds) (1996) Intertidal ecology. Chapman and Hall, LondonGoogle Scholar
  38. Refsnider JM, Janzen FJ (2010) Putting eggs in one basket: ecological and evolutionary hypotheses for variation in oviposition-site choice. Annu Rev Ecol Evol Syst 41:39–57.  https://doi.org/10.1146/annurev-ecolsys-102209-144712 CrossRefGoogle Scholar
  39. Resetarits WJ Jr (1996) Oviposition site choice and life history evolution. Am Zool 36(2):205–215.  https://doi.org/10.1093/icb/36.2.205 CrossRefGoogle Scholar
  40. Richards JG (2009) Metabolic and molecular responses of fish to hypoxia. In: Richards JG, Farrell AP, Brauner CJ (eds) Fish physiology, vol 27. Academic Press, London, pp 443–485Google Scholar
  41. Richards JG (2011) Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J Exp Biol 214(2):191–199.  https://doi.org/10.1242/jeb.047951 CrossRefPubMedGoogle Scholar
  42. Sayer MDJ, Davenport J (1991) Amphibious fish: why do they leave water? Rev Fish Biol Fish 1(2):159–181CrossRefGoogle Scholar
  43. Scherle W (1970) A simple method for volumetry of organs in quantitative stereology. Mikroskopie 26(1):57–60PubMedGoogle Scholar
  44. Smyder EA, Martin KLM (2002) Temperature effects on egg survival and hatching during the extended incubation period of California grunion, Leuresthes tenuis. Copeia 2:313–320.  https://doi.org/10.1643/0045-8511(2002)002%5b0313:TEOESA%5d2.0.CO;2 CrossRefGoogle Scholar
  45. Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr Comp Biol 42(4):780–789.  https://doi.org/10.1093/icb/42.4.780 CrossRefGoogle Scholar
  46. Thomas S, Fievet B, Motais R (1986) Effect of deep hypoxia on acid-base balance in trout: role of ion transfer processes. Am J Physiol 250:R319–R327.  https://doi.org/10.1152/ajpregu.1986.250.3.R319 CrossRefPubMedGoogle Scholar
  47. Todd ES, Ebeling AW (1966) Aerial respiration in the longjaw mudsucker Gillichthys mirabilis (Teleostei: Gobiidae). Biol Bull 130(2):265–288.  https://doi.org/10.2307/1539703 CrossRefGoogle Scholar
  48. Tomanek L, Helmuth B (2002) Physiological ecology of rocky intertidal organisms: a synergy of concepts. Integr Comp Biol 42(4):771–775.  https://doi.org/10.1093/icb/42.4.771 CrossRefPubMedGoogle Scholar
  49. Truchot JP, Duhamel-Jouve A (1980) Oxygen and carbon dioxide in the marine intertidal environment: diurnal and tidal changes in rockpools. Resp Physiol 39(3):241–254.  https://doi.org/10.1016/0034-5687(80)90056-0 CrossRefGoogle Scholar
  50. Vornanen M, Asikainen J, Haverinen J (2011) Body mass dependence of glycogen stores in the anoxia-tolerant crucian carp (Carassius carassius L.). Naturwissenschaften 98:225–232.  https://doi.org/10.1007/s00114-011-0764-5 CrossRefPubMedGoogle Scholar
  51. Yamahira K (1997) Hatching success affects the timing of spawning by the intertidally spawning puffer Takifugu niphobles. Mar Ecol Prog Ser 155:239–248CrossRefGoogle Scholar
  52. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1(1):3–14.  https://doi.org/10.1111/j.2041-210X.2009.00001.x CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Aquatic Behavioural Ecology Laboratory, Department of Psychology, Neuroscience, and BehaviourMcMaster UniversityHamiltonCanada
  2. 2.Department of Collective BehaviourMax Planck Institute for OrnithologyConstanceGermany
  3. 3.Department of BiologyMcMaster UniversityHamiltonCanada

Personalised recommendations